Volitional control of individual neurons in the human brain.

Abstract

Brain machine interfaces allow neuroscientists to causally link specific neural activity patterns to a particular behaviour. Thus, in addition to their current clinical applications, brain machine interfaces can also be used as a tool to investigate neural mechanisms of learning and plasticity in the brain. Decades of research using such brain machine interfaces has shown that animals (nonhuman primates and rodents) can be operantly conditioned to self-regulate neural activity in various motor-related structures of the brain. Here, we ask whether the human brain, a complex interconnected structure of over 80 billion neurons, can learn to control itself at the most elemental scale-a single neuron? We utilized the unique opportunity to record single units in eleven individuals with epilepsy to explore if the firing rate of a single (direct) neuron in limbic and other memory-related brain structures can be brought under volitional control. To do this, we developed a visual neurofeedback task in which subjects were trained to move a block on a screen by modulating the activity of an arbitrarily selected neuron from their brain. Remarkably, subjects were able to volitionally modulate the firing rate of the direct neuron in these previously uninvestigated structures. We found that a subset of participants (learners), were able to improve their performance within a single training session. Successful learning was characterized by 1) highly specific modulation of the direct neuron (demonstrated by significantly increased firing rates and burst frequency), 2) a simultaneous decorrelation of the activity of the direct neuron from the neighbouring neurons, and 3) robust phase-locking of the direct neuron to local alpha/beta-frequency oscillations, which may provide some insights on the potential neural mechanisms that facilitate this type of learning. Volitional control of neuronal activity in mnemonic structures may provide new ways of probing the function and plasticity of human memory without exogenous stimulation. Furthermore, self-regulation of neural activity in these brain regions may provide an avenue for the development of novel neuroprosthetics for the treatment of neurological conditions which are commonly associated with pathological activity in these brain structures, such as medically refractory epilepsy.